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Development of a specific monoclonal antibody based Sandwich ELISA for rapid detection of haemorrhagic septicemia in bovine blood

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As infection with Pasteurella multocida is common in cattle and buffalo, a monoclonal antibody based sandwich ELISA kit was developed for its rapid and easy detection. The test was optimized and standardized so that maximum concordance could be maintained with the standard procedures of hemorrhagic septicemia diagnosis recommended by the WHO expert committee. HS-1, a Pasteurella multocida type B specific monoclonal antibody developed in mice was used as tracing antibody to capture P. multocida serotype B:2 in a sandwich ELISA. The test was standardized for whole killed bacterial cell, sonicated and the LPS antigens of P. multocida type B:2. An anti-pasteurella hyper immune serum raised in rabbit acted as the coating antibody was selected since it was previously shown to be a major immunogen during P. multocida infection in rabbits and contain antibodies against several conserved epitopes. The sensitivity of the sandwich ELISA determined with ELISA well module (8x2) for whole killed bacterial cells, and with two fold serial dilutions of an antigen (12 steps and in triplicate) for sonicated and LPS antigen, were 1.6X1011 cfu/ml, 385 ng/ml and 17.4 mg/ml respectively. Specificity, evaluated against the cultured P. multocida type A antigen of bovine strain, was 100%. The coefficient of variation for sonicated and the LPS antigens calculated from intra and inter plate for same-day and inter-day tests were found within 20% indicating good reproducibility with few exceptions when CV varied more than 20%.

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Original Research Article https://doi.org/10.20546/ijcmas.2019.805.128

Development of a Specific Monoclonal Antibody based Sandwich ELISA for

Rapid Detection of Haemorrhagic Septicemia in Bovine Blood

Ragini Hazari 1* , Arvind Kumar 1 and Sonu Sharma 2

1

Department of Veterinary Microbiology, 2 Department of Veterinary Pathology, Lala Lajpat

Rai University of Veterinary and Animal Sciences, Hisar, Haryana, India

*Corresponding author

A B S T R A C T

International Journal of Current Microbiology and Applied Sciences

ISSN: 2319-7706 Volume 8 Number 05 (2019)

Journal homepage: http://www.ijcmas.com

As infection with Pasteurella multocida is common in cattle and buffalo, a monoclonal

antibody based sandwich ELISA kit was developed for its rapid and easy detection The test was optimized and standardized so that maximum concordance could be maintained with the standard procedures of hemorrhagic septicemia diagnosis recommended by the

WHO expert committee HS-1, a Pasteurella multocida type B specific monoclonal antibody developed in mice was used as tracing antibody to capture P multocida serotype

B:2 in a sandwich ELISA The test was standardized for whole killed bacterial cell,

sonicated and the LPS antigens of P multocida type B:2 An anti-pasteurella hyper

immune serum raised in rabbit acted as the coating antibody was selected since it was

previously shown to be a major immunogen during P multocida infection in rabbits and

contain antibodies against several conserved epitopes The sensitivity of the sandwich ELISA determined with ELISA well module (8x2) for whole killed bacterial cells, and with two fold serial dilutions of an antigen (12 steps and in triplicate) for sonicated and LPS antigen, were 1.6X1011 cfu/ml, 385 ng/ml and 17.4 mg/ml respectively Specificity,

evaluated against the cultured P multocida type A antigen of bovine strain, was 100%

The coefficient of variation for sonicated and the LPS antigens calculated from intra and inter plate for same-day and inter-day tests were found within 20% indicating good reproducibility with few exceptions when CV varied more than 20% In some instances,

CV values as high as 23% and 25% were recorded for whole killed bacterial cell CV values up to 25% indicated repeatability of the ELISA and higher OD values for whole killed bacterial cells did not record high standard deviations (SD) Therefore, the ELISA showed repeatability of the test for all three types of antigens Furthermore, more

expression of the P multocida type B:2 specific PCR in comparison to P multocida type

B and P multocida PCR in early phase of pathogenesis of the disease was detected and showed the greater analytical sensitivity and specificity to identify bovines infected with P multocida The results showed that this sandwich ELISA, with good specificity, sensitivity

and simplicity, would be a useful assay for an early clinical diagnosis of HS The ELISA can be performed directly on infected blood in modestly equipped laboratory, manned by semi skilled personnel

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Introduction

Hemorrhagic Septicemia (HS) is a major

disease of cattle and buffaloes occurring as

epizootics in many Asian and African

countries It is caused by specific serotypes

within the bacterial species of Gram negative

coccobacillary pathogen Pasteurella multocida

viz B:2 and B:5 in Asian counties and type

E:2 in African countries (Carter and De Alwis,

1989) On the basis of capsular antigens, P

multocida has been classified into five

serotypes, namely A, B, D, E and F (Carter,

1955), whereas on the basis of somatic

antigens, it has been classified into sixteen

serotypes (Heddleston et al., 1972) According

to current classification, the family

Pasteurellaceae includes a large group of

Gram negative bacteria that are

chemo-organotrophic, facultatively anaerobic and

fermentative in nature (Mutters et al., 1989) It

is a disease of utmost economic importance

particularly in Asia due to large population of

buffaloes The case fatality rate and

susceptibility to HS are higher in buffaloes

than in cattle (Benkirane and De Alwis, 2002)

HS has been estimated to cause huge economic

losses in India, to the tune of Rs 225 millions

(Singh et al., 2008) However, the losses are

expected to be much greater than that have

been reported because of poor reporting and

surveillance systems

Once clinical signs appear, case fatality is

nearly 100% Variable number of immune

carriers is present in animal populations,

particularly in endemic areas They may be

latent carriers, where the organisms are

lodged in the tonsils, or active carriers, where

organisms are detectable in the naso-pharynx

The long lasting carrier status may escape the

notice of the animal health authorities but

may be of considerable economic significance

(De Alwis, 1981) HS is, typically a

septicemic disease that develops following

release of endotoxin from dead bacterial cells

It has an affinity for respiratory tract mucus

membrane (Lettellier et al., 1991) and a better

affinity for non-ciliated respiratory epithelial cells (Pijoan and Trigo, 1990)

The pathogenic components of P multocida

include capsule, endotoxin and outer membrane proteins which have been reported

to be the virulence factors responsible for immuno-pathological changes (Boyce and

Adler, 2006; Singh et al., 2011)

Regular vaccination at six months interval, before onset of rainy season and beginning of winter, is a major control measure for prevention of HS Various killed vaccines, for example, broth bacterin, aluminum hydroxide precipitated vaccine and the oil adjuvant vaccine, are commonly used for

immunization against HS (Tasneem et al.,

2009) Short duration of immunity of only 4-6 months is a major limitation of the conventional killed bacterial vaccines Oil adjuvanted vaccine induces immunity of little longer duration of about 9 months, yet far lower than that needed (De Alwis, 1992a; OIE, 2012) For improving the duration of immunity, live vaccine with aroA mutant has been experimentally developed and a live

vaccine using deer strain (P multocida B:3,4)

has also been reported (Verma and Jaiswal, 1998) The live vaccine of deer strain is used

only in Myanmar (De Alwis, 1999)

It is a common practice that antibiotics are used to treat the diseased animals HS is a septicemic disease and the animal dies of

endotoxic shock (Horadagoda et al., 2001)

The bacteria multiply fast in the blood of diseased animals and die Release of LPS (endotoxin) from dead bacterial cell causes endotoxic shock and death of the animal Treatment with antibiotics after appearance of clinical signs (fever and recumbency), may hasten the rate of death of bacterial cells in the blood This may further exacerbate the

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condition and hasten the death of animal (De

Alwis, 1999) Inadequate vaccination based

control programme and difficulties of

antibiotic treatment at later stage of the

disease, put emphasis on development of not

only a specific and a sensitive diagnostic test

but use of the test should also reduce time

taken for diagnosis (time spent on collection

and reaching of samples to the lab as well as

time needed to complete the test procedure)

The test of high sensitivity would detect

smaller amount of antigen in clinical samples

and therefore may have capacity for diagnosis

at an early stage, before the onset of clinical

symptoms Point-of-care diagnostics would

reduce the time taken for diagnosis

Therefore, a highly sensitive point-of-care

diagnostics is an ideal test

The polymerase chain reaction (PCR) assay

has been reported for amplification of P

multocida gene, P multocida type B and P

multocida B:2 (Brickell et al., 1998 and

Townsend et al., 1998) PCR is a rapid,

specific and highly sensitive test for

confirmation of HS but it requires

sophisticated laboratory and highly skilled

manpower Therefore, PCR could not be

developed as point-of-care diagnostic test

The PCR can detect even very little amount of

target DNA in the infected blood Despite its

very high sensitivity, time taken for

collection, dispatch and receipt of samples in

laboratory and time taken for completion of

procedure of PCR defeats its use for

diagnosing the disease at an early stage

Attempts have been made to develop simple

agglutination test as point-of-care diagnostic

test Use of agglutinating monoclonal

antibody coated coloured latex beads based

agglutination has given desired sensitivity and

specificity for clinical diagnosis of the disease

(Pankaj Kumar and Arvind Kumar, Indian

Patent Application No 767/DEL/2015 filed

test is not an objective test and therefore, an inexperienced operator may cause error of judgment

It is, therefore necessary to develop simple, accurate and rapid diagnostic test that can be carried out by semi-skilled laboratory personnel even in the modestly equipped laboratories at block or district level ELISA has been successfully used for diagnosis of various bacterial and viral diseases (OIE, 2012) The test can also be converted as a kit for use as point-of-care diagnostics (Anon,

2004, Lister et al., 2012) Dawkins et al.,

(1990) developed an ELISA for detection of

P multocida B:2 However, the test has been

described as a useful tool for screening of bacterial isolates and is based on polyclonal serum Use of polyclonal serum raises a doubt

on specificity of the test Perusal of scientific literature did not show the use of test as field diagnostic test for HS

Monoclonal antibodies have been described

as bio-reagent of unmatched specificity that can distinguish even very closely related micro-organisms and of very high sensitivity because of no undesired cross reactive back ground reactions in ELISA Polyclonal serum may contain antibodies against several conserved epitopes and therefore, polyclonal serum shows cross reactivity in ELISA The conserved epitopes are generally immunodominant epitopes and the epitopes discriminating closely related micro-organisms are immunosubdominant epitopes Low amount of antibody against such immunosubdominant epitopes(s) would lower sensitivity of the test The specificity and sensitivity of the ELISA test are expected to

increase many folds with P multocida B

specific monoclonal antibody and is therefore suitable for early diagnosis of the disease The test could also be converted in to point-of-

care diagnostic test A P multocida B specific

monoclonal antibody has been developed in

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our laboratory (Pankaj Kumar, 2014)

Considering the fact that the matrix of clinical

sample would be the infected blood, a

sandwich ELISA would be more suited for

the purpose The ELISA plate wells coated

with anti-pasteurella multocida polyclonal

serum would selectively capture the P

multocida antigen present in the sample and

then P multocida B specific monoclonal

antibody would bind only to captured P

multocida type B bacteria/antigens This

study is therefore targeted to Development

and optimization of monoclonal antibody

sandwich ELISA for diagnosis of

Hemorrhagic Septicemia of bovines and

evaluation of the test for clinical diagnosis of

Hemorrhagic Septicemia

Materials and Methods

The bacteria

Buffalo calf blood experimentally infected

with P multocida B:2 P52 (Vaccine strain)

was obtained from Haryana Veterinary

Vaccine Institute (HVVI), Hisar The

bacterial stock was prepared by streaking the

infected blood on 5% sheep blood agar and

incubated overnight at 35-36ºC The bacterial

growth on the Petri plate was agar washed

and aliquoted in 50% brain heart infusion

broth (BHI broth) and glycerol The aliquots

were stored at -20ºC The bacteria were

revived as and when required, by streaking on

5% sheep blood agar and incubated overnight

at 35-36ºC For short duration storage of 4-5

days, the bacterial cultures were kept at +4ºC

Buffalo calf blood experimentally infected

with P multocida B:2 P52 (Vaccine strain)

was obtained from Haryana Veterinary

Vaccine Institute (HVVI), Hisar P multocida

type A (bovine strain) was obtained from Indian

Veterinary Research Institute, Izatnagar and

was maintained and cultured Anti-mouse

HRPO conjugate raised in rabbit was

purchased from Sigma Aldrich Co., (cat No.9044) and referred as “The Conjugate” Anti-pasteurella multocida monoclonal antibody referred as “HS-1 Mab” was produced in the department during the doctoral research of Pankaj Kumar (2014) by the hybridoma secreting the monoclonal

antibody and raised in vivo in ascites fluid of

mice, anti- pasteurella multocida whole bacterial cell hyper immune serum named as

“The coating antibody” and raised in rabbit

P multocida type B specific PCR primers

KTSP61 and KTT72 were commercially synthesized from Sigma-Aldrich Chemical Pvt Ltd., Bangalore, India

Experimental animals

Male Swiss albino mice aged 8-10 weeks were procured from Disease Free Small Animal House, Lala Lajpat Rai University of Veterinary & Animal Sciences, Hisar The

mice were caged, fed ad libidum and used

within 2 days of procurement Approval of Institutional Animal Ethics Committee for animal experimentation was granted vide VPHE/IAEC/88-108 dated 19/04/2014

monoclonal antibody sandwich ELISA for diagnosis of hemorrhagic septicemia

A monoclonal antibody based sandwich ELISA was developed and optimized as per the guidelines of OIE (2012) for assay development The test was standardized for: determination of optimum dilutions of the bio-reagents, repeatability, estimation of cutoff, analytical sensitivity and specificity and normalization of data The test was developed

to the extent that it could become fit for clinical diagnosis of experimentally produced

HS in mice Stocks of P multocida B:2 and

P multocida type A were raised and their

Purity, identity was done by using various

biochemical tests viz Catalase test, Oxidase

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test, Indole test, and confirmation was done

by using PCR with KTSP61:5’-

ATC-CGC-TAA-CAC-ACT-CTC-3’ (Tm= 55.00C) (F)

and KTT72:

5’-AGG-CTC-GTT-TGG-ATT-ATG-AAG-3’ (Tm= 61.90

C) (R) primers

Preparation of bacterial antigens

Whole killed bacterial cells antigen, sonicated

antigen and LPS antigen were prepared The

formaldehyde treated A 37% formaldehyde

solution was added to achieve 0.5%

concentration of formaldehyde in The P

multocida B:2 BHI broth A small volume of

5 ml was saved for estimation of colony

forming units (cfu) It was stored at +4OC

overnight and used next day for estimation of

cfu

The whole killed bacterial cell antigen

Of the 195 ml The P multocida B:2 BHI

broth of inactivated bacteria, approximately

50 ml broth was used It was pelleted by

centrifugation at 3000 rpm (swing out rotor,

Remi centrifuge model no R-4CDx

Laboratory centrifuge) Supernatant was

discarded and bacterial pellet was suspended

in 20 ml phosphate buffer saline (PBS-T) It

was stored at +4ºC till use

Estimation of colony forming units

Limiting dilution method was used (Prescott

et al., 2002) The dilution that produced

about 20-30 bacterial colonies on the Petri

plate was considered for estimation of cfu in

The P multocida B:2 BHI broth

The sonicated bacterial antigen

Approximately 100 ml of The P multocida

B:2 BHI broth was centrifuged as described

above Supernatant was discarded and pellet

was suspended in about 30 ml PBS-T The bacterial cells were disrupted by ultra sonication (ultra sonication model ultrasonicator-Micronix S-4000 micronix) as per standard procedure and the supernatant was saved and stored at -20oC till use This way sonicated bacterial antigen was prepared

Estimation of protein concentration of sonicated antigen

Estimation of protein concentration of sonicated antigen was done as per the method described by Bradford (1976) by using Coomassie Blue G-250 The absorbance of the sample at 595 nm was taken and the protein concentration was determined from the standard curve

The LPS antigen

Bacterial LPS antigen was prepared as

described by Pandian et al., (1999) A total of

45 ml of The P multocida B:2 BHI broth was

used for preparation of LPS antigen

Estimation of carbohydrate concentration

of LPS antigen

The amount of carbohydrate was estimated

for determination of analytical sensitivity of The ELISA test of LPS antigen It was done

by sulphuric acid-UV method using the regression equation as described by

Albalasmeh et al., (2013)

Assay development and validation

Sandwich ELISA was developed and optimized The ELISA plate wells were coated with the coating antibody The coating antibody captured the antigen Then antigen was detected by the HS-1 Mab The binding

of the HS-1 Mab with the captured antigen was detected by the conjugate and finally the test was developed with 3,3,5,5, Tetra Methyl

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Benzidine (TMB) The optical density of the

colour (OD value) was recorded in an ELISA

reader at filter wave length 450 nm The test

was standardized and optimized for all three

types of antigens (whole killed bacterial cell

antigen, sonicated antigen and the LPS

antigen)

For the sandwich ELISA, the wells of a 96

well flat bottom ELISA plate (Maxisorp,

Nunc) were coated with 50µl/well of

appropriate dilution of the coating antibody

prepared in coating buffer The plate was

covered and kept at +40C overnight Next day,

the plate wells were washed with washing

buffer (PBS-TT) and then discarded by flick

of wrist This was done 5X

The wells of the plate were blotted dry This

way washing and drying of the ELISA plate

wells were done Antigen was diluted in

diluent and appropriately diluted antigen was

added as 50µl/ well The plate was covered

with plate cover and then incubated 35-360C

for 1h The wells of the plate were again

washed and dried as described above

Appropriately diluted HS-1 Mab, was added

as 50µl/ well and ELISA plate incubated as

described above The plate wells were washed

as done above and appropriately diluted

conjugate was added as 50µl/ well The plate

was again incubated, washed and dried as

described above

To develop the test, TMB solution was added

as 50µl/ well The colour was allowed to

develop for 7-8 min and then the reaction was

stopped by acidification The stopping solution

was added 50µl/ well The OD values were

read at 450 nm wave length This is described

as, “The ELISA test.”

In each setup of the ELISA, appropriate

control was kept The controls were set up as

blank, negative and positive controls as

required in an experiment

Standardization of the test

Chequer board titration was performed for

standardization of the test This was done for determination of optimum dilutions of: 1- The coating antibody, 2- HS-1 Mab and 3- The conjugate The optimum dilutions were determined for 1:5, 1:50 and 1:100 dilutions of antigens

A 96 well ELISA plate (Nunc) was divided in

to four parts The coating antibody was fold diluted column-wise (1:125 to 1:1000, 4 steps) and the conjugate diluted two fold row-wise (1:200 to 1:6400, six steps) A dilution

two-of HS-1 Mab was added to wells two-of one two-of four parts of the plate The dilutions of HS-1 Mab used were 1:500, 1:800, 1:1000 and 1:1500 Layout of ELISA plate is shown in Figure 11 Combination of the most diluted coating antibody, HS-1 Mab, The conjugate and the antigen in a well showing appreciable colour development (at least, OD 0.2) taken

as optimum dilution of The coating antibody, HS-1 Mab and The conjugate

The repeatability studies

For testing the robustness of the test, repeatability study was performed The experiment was set up as described in OIE (2012) However, 24 replicates of each three

dilutions of an antigen (1:5, 1:10, 1:50) were

kept in the ELISA plate These way three plates were set up and the experiment was

repeated in similar manner on three different

days

Statistical analysis

Mean and standard deviations (SD) of OD values of the wells: intra-plate, inter-plate and inter-days were calculated in MS Excel 2007 From the values of mean and SD, coefficient

of variation (CV) was calculated by dividing

SD over mean (CV= SD/mean) The CV(s)

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were calculated for all the three dilutions of

all the three antigens

Estimation of cut off value

Cut off value is determined to establish

criterion for declaring a test positive or

negative In the study, mean + 3SD of OD

value negative control wells were taken as cut

off value The ELISA was set up with two

different types of negative control wells In

one type of negative control wells, only

diluent was added and no antigen was added

In the second type of negative control wells,

an antigen of P multocida B:2 was added but

an ascites fluid containing unrelated

monoclonal antibody was used The ELISA

test was performed with all three types of the

P multocida B:2 antigens The ELISA test

conditions were kept same as standardized for

a type of P multocida B:2 antigen For the

ascites of unrelated monoclonal antibody, the

dilution of the ascites fluid was kept similar to

the dilution of HS-1 Mab for that type of P

multocida B:2 antigen

Analytical sensitivity

Analytical sensitivity is the lowest amount of

analyte that can be detected by the test For

estimation of analytical sensitivity of The

ELISA standardized for all three types of

antigens The ELISA test was performed with

two fold serial dilutions of an antigen (12

steps and in triplicate) but for whole killed

bacterial cell antigen it was performed in the

ELISA well module (8X2) The highest

dilution of antigen recorded OD value equal

to the cut off value was taken as the ELISA

titre The dilution of the ELISA titre was used

to estimate the amount of an antigen in that

dilution The amount of antigen in stock of

whole killed bacterial cell, sonicated and the

LPS were estimated as described in sections

3.6.2.1a, 3.6.2.2a, 3.6.2.3a respectively

Amount of antigen in stock was divided by

the dilution of the ELISA titre to calculate amount of antigen in 50µl volume of the antigen dilution This way analytical sensitivity of the ELISA for all three types of antigen was established

Analytical specificity

Analytical specificity is the degree to which the assay does not cross react with other analyte Analytical specificity of The ELISA

test was established against P multocida type

A antigen of bovine strain and the ELISA test

was performed with a change that P

multocida type A antigen was used in place of

P multocida B:2 antigen The ELISA was

done with all three types of the antigens (whole bacterial cell killed, sonicated and the

LPS antigen of P multocida type A) The

ELISA test conditions were kept same as

standardized for P multocida B:2 antigens

For a type of antigen, all optimum dilutions of The coating antibody, HS-1 Mab and The conjugate were kept same as standardized for

that type of P multocida B:2 antigen The

whole killed bacterial cell antigen was used as undiluted stock of the bacterial culture while sonicated and the LPS antigen was used in dilution 1:5 Though, amount of protein in sonicated antigen, and carbohydrate in the

LPS antigen of P multocida type A culture

broth were not estimated but the number of cfu were estimated and the dilution of the stock culture in BHI broth was so adjusted that the number of cfu in the BHI broth of

both P multocida B:2 and P multocida type

A became similar in number This was done

to have amount of protein in sonicated antigen and carbohydrate in LPS almost similar to the

antigen of P multocida B:2 The number of cfu in stock culture of P multocida type A were higher than that in stock culture of P

multocida B:2 The stock culture of P multocida type A was, therefore, appropriately diluted and then the whole killed bacterial cell, sonicated and the LPS

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antigens of P multocida type A were

prepared respectively, for P multocida B:2

Four replicates of a type of the antigen of P

multocida type A were tested together

positive control In positive control, another

anti-pasteurella multocida monoclonal

antibody that cross reacts equally with P

multocida B:2 and P multocida type A

(Pankaj Kumar,2014) was used The dilution

of the cross reacting monoclonal antibody

was kept similar to the dilution of HS-1 Mab

standardized for a type of antigen

Normalization of data

To minimize test to test variations,

normalization of the data was done The OD

value of test well could either be converted as

percentage of reaction in comparison to OD

value of known positive control or it could be

expressed as ratio of test well OD value over

negative control well OD value In the study,

ratio of test well OD over mean +3SD value

of negative control wells OD was used for

normalization of data

Evaluation of the test for clinical diagnosis

of HS

The ELISA test standardized and optimized

with laboratory prepared P multocida B:2

antigens was assessed for its fitness as test for

clinical diagnosis of the disease The test was

evaluated not only for its fitness for clinical

diagnosis of HS but also its capacity to

diagnose the disease at an early stage, before

the appearance of clinical symptoms The

bacteria could be in any of the three forms i.e

whole bacterial cell, disintegrated bacterial

cell and LPS The sonication mimicked the

disintegration of the bacterial cell While,

whole bacterial cell is expected in the early

stages of the disease, protein and LPS

antigens of disintegrated bacteria are likely to

be present in samples collected from animals

with clinical symptoms or died of HS The

ELISA test was developed for all three types

of antigens but the ELISA test developed for whole killed bacterial cell was used This was done to assess the capacity of The ELISA test for early diagnosis of HS

A total of 9 mice were experimentally

infected with P multocida B:2 P52 strain by

s/c inoculation of 0.5 ml BHI broth containing

100 cfu One mouse was kept as non-infected control The control mouse received 0.5ml

BHI broth without P multocida B:2

The heart blood of the infected mice was collected at 2, 4, 8, 12 and 24 h post infections The surviving mice were killed by cervical dislocation and heart blood was collected directly by puncturing the heart Two mice were used at each sampling except The heart blood of the non-infected mouse was collected at the time of sampling at 24 h post infection

Isolation of bacteria from clinical samples

The Isolation of bacteria, ELISA test and PCR were performed on the collected blood samples The control mouse was killed by cervical dislocation The blood samples at various time post infections were tested by The ELISA test as standardized for whole killed bacterial cell was setup The ELISA test results were compared with “Gold standard’ of HS diagnosis The heart blood samples of various time post infections were tested for isolation of bacteria and for the detection of the bacterial DNA by PCR Heart blood of individual infected mouse, at various sampling, was streaked on a 35 mm 5% sheep blood agar Petri plate for isolation of the bacteria and the heart blood of two mice at a sampling time was pooled and then used for detection of the target bacterial DNA by PCR The pooled blood samples were also used in The ELISA test

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The ELISA test

The ELISA test was performed with the

optimum dilutions 1:1000, 1:500 and 1:800 for

the coating antibody, HS-1 Mab and The

conjugate, respectively Two dilutions of the

blood samples (Undiluted and 1:2 diluted) were

tested The heart blood collected at all the

sampling time, was hemolysed by adding

distilled water three times This was done to

remove any interference of red blood cells in

antigen binding Approximately 100µl of blood

could be collected from each mouse and it could

be suitably hemolysed with distilled water

resulting in to1:3 dilution of the blood This 1:3

diluted blood sample was used as undiluted

blood sample The mice at 24 h post infection

died much before the time of sampling (during

very early hours of morning) Very little amount

of heart blood could be collected As such there

was no blood sample, therefore heart was cut

and little heart blood samples whatever amount,

could be collected by washing the thoracic

cavity with 0.3 ml distilled water The prior

dilution of this heart blood sample of 24 h in

undiluted blood, could not be determined The

samples appeared to be highly diluted (Fig 1

and 2) The layout of ELISA well module is

shown in Figure 11 and OD values of heart

blood samples are shown in Table 1

The PCR

The PCR was performed on undiluted as well as

diluted blood samples (Table 2) The P

multocida gene specific PCR performed on

direct blood samples showed positive

amplification in the samples collected 4 and 8 h

post infection No amplification was recorded

for heart blood sample of 12 and 24 h post

infection

Detection of target DNA in infected mice

blood by PCR

P multocida gene specific, as well as duplex

PCR for amplification of P multocida type

and P multocida B:2 were set up P

multocida, serogroups B and type B:2 specific

multiplex-PCR was used to confirm the

strains as P multocida type B:2 Different

sets of primers specific to capsule as well as 16s RNA were used as mention in the (Table 3)

PCR parameters

Three PCR were performed i.e simplex, duplex and multiplex Simplex PCR using KMT1T7 and KMT1SP6 set of primer

specific to P multocida, duplex PCR for simultaneous detection of P multocida Type

B using two sets of primer i.e

KMT1T7/KMT1SP6 and KT SP61 /KTT72

however, multiplex PCR using three sets of

primer for simultaneous detection of P

multocida Type B:2 were used

The PCR was performed in a thermocycler (Veriti, Invitrogen) with a total reaction volume of 25 µL using KAPA blood PCR kit (KK7003)

Results and Discussion

Culture of P multocida

The bacteria were streaked on 5% sheep blood agar Petri plate Characteristic translucent dew drop like colonies appeared after incubating overnight at 35-36oC Gram’s staining of the bacterial smear showed Gram negative small cocco-bacilli appearance Presence of only gram negative small cocco-bacilli bacteria in the smear, indicated purity

of the culture (Fig 3)

P multocida was identified by various

biochemical tests (Table 3) and P multocida type B was confirmed by PCR The PCR

showed amplification of target DNA (Fig 4) showing a band of amplicon size of ~620 base pairs (bp)

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Preparation of bacterial antigens

No bacterial growth was observed, after

overnight incubation of P multocida B:2

broth

Estimation of colony forming units

The number of colonies on the Petri plate was

30, 24 and 27, inoculated with dilution 10-12

of the broth of bacterial culture (Fig 5) and

therefore the Petri plates of 10-12 gave an

average of 27 bacterial colonies

The BHI broth of the bacterial culture

contained 27X10-12 cfu in 50µl or 54X10-13

cfu per ml of The P multocida type B:2 BHI

broth

This was expected to be an accurate

estimation of the bacterial antigen because the

bacterial culture was terminated at 8 h, during

log phase of the bacterial growth In over

grown bacterial culture, the culture might

contain dead bacterial cell and cfu may not be

the correct estimation of whole cell bacterial

number

Estimation of protein concentration of

sonicated antigen

The standard curve (Fig 6) was made using

bovine serum albumin with concentrations of

0, 10, 20, 30, 40, 50 µg/ml for the microassay

(extinction coefficient of BSA is 0.667)

Protein concentration of sonicated antigen

was estimated from standard curve with

absorbance at 595nm It was estimated to be

44 µg/ml

Estimation of carbohydrate concentration

of LPS antigen

The stock concentration of LPS antigen

estimated by sulphuric acid-UV method was

1.392g/ml

Assay development and validation

Sandwich ELISA was standardized for all three types of antigens by performing Chequer board titration to determine the optimum dilutions of: 1-The coating antibody, 2-HS-1 Mab and 3-The conjugate The optimum dilutions of antigens were taken as 1:5, 1:50 and 1:100

Chequer board titration for whole killed bacterial cell antigen

Raw OD values recorded for antigen concentration 1:5, 1:50 and 1:100 in Chequer board titrations are shown in (Tables 4, 5 and 6), respectively

The ELISA plate OD values for antigen dilution 1:50 were used for determination of optimum dilutions The Optimum dilutions of bio-reagent were selected as the coating antibody- 1:1000, HS-1 Mab-1:500 and the conjugate-1:800

Chequer board titration for sonicated antigen

Raw OD values recorded in Chequer board titrations for antigen concentration 1:5, 1:50 and 1:100 are shown in (Tables 7, 8 and 9), respectively The ELISA plate OD values for antigen dilution 1:100 were used for determination of optimum dilutions The Optimum dilutions of reagent were selected as: The coating antibody- 1:1000, HS-1 Mab-1:1500 and the conjugate-1:6400

Chequer board titration for LPS antigen

Raw OD values recorded for antigen concentration 1:5, 1:50 and 1:100 are shown

in (Tables 10, 11 and 12), respectively

The ELISA plate OD values for antigen dilution 1:5 were used for determination of

Trang 11

optimum dilutions The Optimum dilutions of

reagent were selected as: The coating

antibody- 1:1000, HS-1 Mab-1:1500 and the

conjugate-1:3200

Repeatability study

Three plates on three days with 24 replicates of

one antigen dilution in one plate were set up

Repeatability of the test was estimated from

calculation of coefficient of variation (CV) from

OD values The experiments were performed

for all three types of antigens and the values

of estimated CV are given in (Tables 13, 14,

15) for whole killed bacterial cell, sonicated

and LPS antigens, respectively The CV

estimated for intra-plate, inter plate and inter

days for all three antigens were largely within

20% For some ELISA plate, the values of

CV was slightly above than 20% but below

21% This was due to rounding off values

during calculation However, 23 % and as

high as 25 % was recorded for whole killed

bacterial cell antigen only

Estimation of cut off value

Cut off values were estimated for declaring

positive or negative result The mean +3SD

values calculated for all three types of antigen

and for both formats of negative control

wells, are given in (Table 16) The cut off

value for whole killed bacterial cell, sonicated

and LPS antigens were found to be 0.11,

0.086 and 0.1, respectively

Analytical sensitivity

The ELISA was performed with various two

fold dilutions of an antigen The highest

dilution of the antigen where OD value

equivalent to cut off OD values, was recorded

as ELISA titre The OD values were plotted in

MS Excel 2007 and exact dilution

corresponding to the cut off values was

estimated for the ELISA titre (Fig 7, 8 and 9)

for whole killed bacterial cell, sonicated and LPS antigen, respectively

OD values with whole killed bacterial cell, sonicated and LPS antigens are given in (Tables 17, 18 and 19) respectively The ELISA titres for whole killed bacterial cell, sonicated and LPS antigen were 1:320, 1:114 and 1:80, respectively Amount of antigen were: 5.4X1014cfu per ml, 44µg per ml and 1.392g per ml for whole killed bacterial cell, sonicated and LPS antigen, respectively Therefore, the analytical sensitivity for whole killed bacterial cell was 1.6X1011cfu/ml, 385ng/ml for sonicated antigen and 17.4mg/ml for LPS antigen

Analytical specificity

High OD values in positive control wells and

OD values close to zero in wells of P

multocida Type A bovine strain (Table 20)

established the analytical specificity of the

test for P multocida type B against most

closely related bacteria

Standardized ELISA for clinical diagnosis

1 Mab and The conjugate, respectively

Isolation of bacteria from clinical samples for evaluation of the test

The bacterial growth was observed with 20 colonies in the blood samples taken after 8 h and 45 colonies 12 h while no discrete colony was seen in the culture of blood sample of 24

h The bacteria were identified as P

multocida by appearance in Gram’s stain

smears

Trang 12

The ELISA test

The ELISA test was performed with the

optimum dilutions 1:1000, 1:500 and 1:800

for the coating antibody, HS-1 Mab and The

conjugate, respectively Two dilutions of the

blood samples (Undiluted and 1:2 diluted)

were tested.The layout of ELISA well module

is shown in Figure 11 and OD values of heart

blood samples are shown in Table 21

The PCR

The PCR was performed on undiluted as well

as diluted blood samples The P multocida

gene specific PCR performed on direct blood

samples showed positive amplification in the

samples collected 4 and 8 h post infection No

amplification was recorded for heart blood

sample of 12 and 24 h post infection The PCR

for duplex amplification of P multocida B and

serotype B:2 specific gene performed on blood

samples showed positive amplification in

samples collected 4, 8 and 12 h post infection

but the lane no.7 of (Fig 10) for samples

collected 24 h post infection showed smearing

This indicated high amount of template

bacterial DNA in the sample of 24 h post

infection

The blood sample of 24 h post infection was

further three fold diluted to lower the amount

of template DNA and then PCR for duplex

amplification of P multocida B and serotype

B:2 specific gene was performed Positive

amplification could be noted in samples

collected 8, 12 and 24 h post infection The

sample of 8 and 12 h post infection showed

amplification for both P multocida B and

sero type B:2 specific genes The samples at

24 h post infection showed amplification of

only P multocida serotype B:2 specific gene,

lane no.6 of (Fig 10) The target bacterial

DNA, therefore, could be detected in heart

blood samples of 4, 8, 12, and 24 h post

infection

isolation, ELISA and PCR for the samples

of experimentally infected mice

The results of isolation of bacteria, The ELISA test and PCR on heart blood samples

of experimentally infected mice are given in (Table 20 and 21)

The ELISA recorded positive results even in 2

h post infection but PCR tested positive in 4 h sample and bacteria started appearing at 8 h post infection The OD values in test wells of infected blood samples demonstrated much higher value when compared with heart blood

of non-infected mouse The OD values in both undiluted and diluted heart blood samples demonstrated an increasing trend from 2 h onwards to 12 h However, lower

OD values were recorded in samples of 24 h post infection

Prompt diagnosis of bacterial infectious diseases of livestock is an important step in management of outbreaks In many developing or underdeveloped Asian countries, including India, an effective vaccination based control programme is not in place This is due to poor animal husbandry conditions as a result of lack of facilities, non-cooperative attitude of livestock owners due

to ignorance and poor knowledge For diseases that occur on an outbreak scale and

an effective vaccine is also available for their successful prevention, even then veterinary health personnel are compelled to adopt approach of treatment of diseased animals with antibiotics In India, this approach of antibiotics treatment and not prevention of the disease by regular vaccination with wider coverage is a common practice for tackling

HS Per acute nature of the disease results in

to very short course of the disease and the fact that antibiotic treatment is disadvantageous at later stage of the disease, there is very little time available with veterinarians to start the

Trang 13

treatment of diseased animals with antibiotics

Treatment with antibiotics is of limited value

unless carried out in the very early stages

(Buxton and Fraser, 1977) Huge economic

losses, predominantly, due to death of young

adult buffaloes creates a panic and often

antibiotic treatment is started without

confirmation of the disease The

indiscriminate use of antibiotics leads to

emergence of resistance in bacteria, undue

contamination of the environment and the life

of the animal is also not saved and money of

livestock owner is wasted on purchase of

expensive antibiotics It is therefore demand

of time that, sensitive, specific, point-of care

and affordable diagnostics should be available

to veterinarians

Importance of diagnostics led to focus of

researchers on developing newer and better

diagnostics This resulted in to rapid

advancement in techniques and technology of

disease diagnosis

In the present study, a monoclonal antibody

based sandwich ELISA was developed for

HS An anti-pasteurella multocida B:2 strain

P52 (vaccine strain) whole bacterial cell

polyclonal serum was used as capture

antibody The immune response to whole

bacterial cell involved the activation of

multiple B-cell which target a specific epitope

on the bacterial cell As a result, a large

number of antibodies were produced with

different specificities and epitope affinities In

contrast, monoclonal antibodies are antibodies

produced by a single B lymphocyte clone As

most monoclonal antibodies lose some or all

of their binding affinity when adsorbed on

plastic, there is an advantage in coating with

polyclonal antibodies because at least some of

the population of antibodies retain binding

activity when adsorbed (Wild and Kusnezow,

2005) Considering the advantages of

polyclonal serum as capture antibody, the

anti- pasteurella whole bacterial cell

polyclonal serum was used as capture antibody and the HS-1 Mab was used as tracing antibody Though, the polyclonal

serum would capture P multocida or other bacterial antigen close to the P multocida,

however, specificity of the test would be maintained The tracing monoclonal antibody,

being P multocida B specific, would bind only to captured P multocida type B

The objective of the research was not only to develop a specific ELISA for HS but the test should have the capacity for early diagnosis

of the disease For this reason, the standardized ELISA was applied on samples collected at different hours post infection of experimentally infected mice The blood samples of as early as 2 h post infection were tested for presence of the bacterial antigen The clinical manifestations of the typical HS disease caused by B:2 or E:2 strains include a rise in temperature, respiratory distress with nasal discharge, and frothing from the mouth, leading to recumbency and death Septicemia

is the characteristic feature in all the disease conditions The incubation period varies from

3 to 5 days In peracute cases, sudden death with observable clinical signs may be observed (Carter and De Alwis, 1989) and De Alwis (1992b) Characteristic of sudden onset

of disease leading to rapid death of infected animals is similar to that seen in other clinical conditions known to involve endotoxic shock

(Radostits et al., 2007) Horadagoda et al.,

(2001) studied role of endotoxin in the pathogenesis of hemorrhagic septicemia in buffaloes The findings demonstrated that a progressive endotoxaemia and associated sequel, correlates with the development of overt hemorrhagic septicemia disease and sudden death in buffaloes It was, therefore, expected that the antigens of three types i.e whole bacterial cells, disintegrated bacterial cells due to death of bacteria and the LPS released from the dead bacterial cells are likely to be present in the clinical sample In

Trang 14

view of this, ELISA was standardized for

whole killed bacterial cells, sonicated

bacterial cells antigen and the LPS antigen

During the standardization of ELISA, it was

observed that The ELISA test, with sonicated

antigen performed better than whole killed

bacterial cell and the LPS antigen because, for

sonicated antigen, the ELISA plate OD values

for antigen dilution 1:100 were used for

determination of optimum dilutions The

optimum dilutions of reagent were selected

as: The coating antibody- 1:1000, HS-1 Mab-

1:1500 and the conjugate-1:6400 Though, for

the LPS antigen, higher optimum dilutions of

bio-reagents: The coating antibody-1:1000,

HS-1Mab-1:1500 and The conjugate-1:3200

were selected but, the test for LPS could be

performed with 1:5 dilutions of antigen only

and the OD value of selected well was also

0.206, just reaching to the minimum

acceptable OD value as describe in section

3.6.3.1 For sonicated antigen, the selected

antigen dilution was 1:100 and the OD value

of the selected well was 0.840, much higher

than the OD value of 0.206 for LPS antigen

The physical form of the antigen influences

how one detects its reaction with an antibody

If the antigen is a particulate, one generally

looks for agglutination of the antigen by the

antibody If the antigen is soluble one

generally looks for the precipitation of the

antigen after the production of large insoluble

antigen-antibody complexes (Mayer, 2013)

Lower performance of the test for whole

killed bacterial cell antigen was, therefore,

due to physical form of the antigen and the

soluble form of antigens in sonicated and the

LPS antigen preparations performed better

The ELISA test could perform only in lower

dilution of the LPS antigen (1:5 dilution)

This was, perhaps, due to lower amount of the

antigen in the LPS antigen preparations The

epitope of the HS-1 Mab has been reported to

be present on fimbriae (Pankaj Kumar, 2014)

Extraction of LPS from bacterial cells would

have been satisfactory, but the epitope of the HS-1 Mab is not present on LPS or outer membrane proteins co-extracted with LPS

Purified LPS of P multocida has been

reported to be non protective and it was concluded that LPS preparation contaminated with outer membrane protein could afford protection (Muniandy and Mukkur, 1993) It appeared that, some amount of fimbrial antigen was co-extracted with the LPS Being

a soluble antigen, it could perform better in ELISA and therefore, higher optimum dilutions of bio-reagents were selected but being low in amount in LPS antigen preparation, it could work only in lower dilution of the LPS antigen

The test is considered a repeatable test if CV

is within 20% The ELISA test was found to

be a repeatable test with few exceptions when

CV varied more than 20% For most ELISA test the CV recorded beyond 20% in decimals only and it was due to rounding off during calculations In some instances, as high as 23% and 25% CVs were also recorded However, higher percentages of CVs were not due to higher values of standard deviations but due to lower mean values The CV is calculated by dividing SD by mean value The test could be considered a poorly repeatable test only if value of standard deviation is high Analytical sensitivity for whole killed bacterial cell was 1.6X1011cfu/ml, 385ng/ml for sonicated antigen and 17.4mg/ml for LPS antigen The analytical sensitivity of whole killed bacterial cell and the sonicated antigen are of more relevance for standardization of test as diagnostic test of HS This is because

of the fact that the fimbrial antigens are likely

to be present in whole killed bacterial cell and

in sonicated antigen preparations

It has been reported that 1.6X109 cfu

Escherichia coli (Tanner, 1948) would weigh

a gram and therefore, 385ng of the sonicated

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